Spatial Mnemonic Encoding: Theta Power Decreases and Medial Temporal Lobe BOLD Increases Co-Occur during the Usage of the Method of Loci

Abstract

The method of loci is one, if not the most, efficient mnemonic encoding strategy. This spatial mnemonic combines the core cognitive processes commonly linked to medial temporal lobe (MTL) activity: spatial and associative memory processes. During such processes, fMRI studies consistently demonstrate MTL activity, while electrophysiological studies have emphasized the important role of theta oscillations (3-8 Hz) in the MTL. However, it is still unknown whether increases or decreases in theta power co-occur with increased BOLD signal in the MTL during memory encoding. To investigate this question, we recorded EEG and fMRI separately, while human participants used the spatial method of loci or the pegword method, a similarly associative but nonspatial mnemonic. The more effective spatial mnemonic induced a pronounced theta power decrease source localized to the left MTL compared with the nonspatial associative mnemonic strategy. This effect was mirrored by BOLD signal increases in the MTL. Successful encoding, irrespective of the strategy used, elicited decreases in left temporal theta power and increases in MTL BOLD activity. This pattern of results suggests a negative relationship between theta power and BOLD signal changes in the MTL during memory encoding and spatial processing. The findings extend the well known negative relation of alpha/beta oscillations and BOLD signals in the cortex to theta oscillations in the MTL.

Keywords: EEG; fMRI; memory encoding; method of loci; mnemonics; theta oscillations.

Figure 1.

Memory encoding paradigm. A, B, Participants were trained to use two mnemonic encoding strategies: the spatial method of loci (A) and the nonspatial pegword method (B). In both methods, participants have to link internal cues, which are either familiar waypoints or associations of items to numbers, to items presented during the encoding phase. During each encoding phase, lists of 20 words were presented sequentially followed by a distracter task and a free recall phase. C, The whole experiment entailed a training phase the day before and 12 encoding–recall cycles during EEG or fMRI recordings.

Figure 2.

Memory performance: the percentage of recalled words in the spatial and nonspatial encoding condition during the EEG experiment and fMRI experiment. In both datasets, memory performance was higher using the spatial method of loci mnemonic. Error bars show the SEM.

Figure 3.

EEG sensor level results. A, A cluster permutation statistic restricted to the theta frequency range revealed ongoing decreases in theta oscillatory power for spatial mnemonic processing in contrast with nonspatial processing, and item-related theta power decreases correlating with successful memory formation. The time–frequency plots show the t-sum values across electrodes of the significant clusters at every time–frequency bin to visualize the extent of the three-dimensional clusters. B, Additional increases in alpha/beta power during spatial encoding and memory formation were evident after word presentation. Time–frequency plots here show p values of a sliding cluster statistic (i.e., separately calculated cluster permutation tests of each time–frequency bin). C, Topographies of theta and alpha/beta power effects of a cluster statistic for the average power for time–frequency windows highlighted in B (dashed boxes) are plotted below, circles highlight electrodes belonging to significant clusters. Warm colors indicate increases in power for spatial processing and successfully encoded items, cold colors indicate decreases in power for spatial processing and successfully encoded items in contrast to nonspatial processing and subsequently forgotten items, respectively.

Figure 4.

fMRI results for spatial vs nonspatial contrasts and memory effects. A, A region of interest analysis was performed for MTL regions, revealing increases in activity for the spatial mnemonic and successful memory formation (p < 0.001, cluster size >10). B, C, An exploratory whole-brain analysis revealed additional effects in typical spatial cortical networks (i.e. retrosplenial cortex, bilateral MTL, B) and memory related regions (i.e., left inferior frontal gyrus, C; p < 0.001, all p < 0.05 FWE cluster level). Warm colors indicate higher BOLD signals for spatial processing and later remembered items; cold colors indicate higher BOLD signals for nonspatial processing and subsequently forgotten items.

Figure 5.

Theta power changes in MTL. A, MTL region of interest consisting of parahippocampal gyrus and hippocampus, highlighted here in green (right MTL) and yellow (left MTL). Virtual electrodes were placed in the same ROIs as in fMRI ROI analysis (Figs. 4A, 7). B, Theta power effects of virtual electrodes in left and right MTL: theta power decreases were found bilaterally for spatial vs nonspatial processing and left lateralized for successful memory formation. Nonsignificant time–frequency bins are whitened.

Figure 6.

EEG source localization results. A, Decreases in theta power for spatial processing were strongest in anterior MTL areas, Alpha/beta power increases were strongest in occipital–parietal–temporal areas for spatial vs nonspatial processing. B, Theta power decreases during successful memory formation were strongest in left temporal areas. Increases in alpha/beta power during memory formation were found in occipital–parietal areas. All plots are thresholded at half-maximum t value.

Figure 7.

Theta EEG power and fMRI beta weights of the left MTL ROI. Theta power (3–7 Hz, −1 to 3 s) and beta weights were averaged for each condition for all voxels included in the anatomically defined left MTL ROI. Theta power decreases show the reversed pattern of BOLD increases in left MTL regions. Error bars show the SEM.